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of Somatosensory Orthoses on Postural Control (A Pilot Study)
Emma Dupuy, Pascale Leconte, Elodie Vlamynck, Audrey Sultan, Christophe Chesneau, Pierre Denise, Stéphane Besnard, Boris Bienvenu, Leslie M. Decker
To cite this version:
Emma Dupuy, Pascale Leconte, Elodie Vlamynck, Audrey Sultan, Christophe Chesneau, et al..
Ehlers-Danlos Syndrome, Hypermobility Type: Impact of Somatosensory Orthoses on Postural Con-
trol (A Pilot Study). Frontiers in Human Neuroscience, Frontiers, 2017, 11, pp.283. �10.3389/fn-
hum.2017.00283�. �hal-02135274�
Ehlers-Danlos Syndrome,
Hypermobility Type: Impact of
Somatosensory Orthoses on Postural Control (A Pilot Study)
Emma G. Dupuy
1, Pascale Leconte
1, Elodie Vlamynck
1, Audrey Sultan
1,2, Christophe Chesneau
3, Pierre Denise
1, Stéphane Besnard
1, Boris Bienvenu
1,2and Leslie M. Decker
1*
1
COMETE, INSERM, UNICAEN, Normandie Université, Caen, France,
2Department of Internal Medicine, University Hospital Center of Caen, UNICAEN, Normandie Université, Caen, France,
3LMNO, CNRS, UNICAEN, Normandie Université, Caen, France
Edited by:
Alain Hamaoui, Jean-François Champollion University Center for Teaching and Research, France
Reviewed by:
Arnaud Saj, Université de Genève, Switzerland Sébastien Caudron, Université de Lorraine, France
*Correspondence:
Leslie M. Decker leslie.decker@unicaen.fr
Received: 27 January 2017 Accepted: 15 May 2017 Published: 08 June 2017 Citation:
Dupuy EG, Leconte P, Vlamynck E, Sultan A, Chesneau C, Denise P, Besnard S, Bienvenu B and Decker LM (2017) Ehlers-Danlos Syndrome, Hypermobility Type:
Impact of Somatosensory Orthoses on Postural Control (A Pilot Study).
Front. Hum. Neurosci. 11:283.
doi: 10.3389/fnhum.2017.00283
Elhers-Danlos syndrome (EDS) is the clinical manifestation of connective tissue disorders, and comprises several clinical forms with no specific symptoms and selective medical examinations which result in a delay in diagnosis of about 10 years. The EDS hypermobility type (hEDS) is characterized by generalized joint hypermobility, variable skin hyperextensibility and impaired proprioception. Since somatosensory processing and multisensory integration are crucial for both perception and action, we put forth the hypothesis that somatosensory deficits in hEDS patients may lead, among other clinical symptoms, to misperception of verticality and postural instability. Therefore, the purpose of this study was twofold: (i) to assess the impact of somatosensory deficit on subjective visual vertical (SVV) and postural stability; and (ii) to quantify the effect of wearing somatosensory orthoses (i.e., compressive garments and insoles) on postural stability. Six hEDS patients and six age- and gender-matched controls underwent a SVV (sitting, standing, lying on the right side) evaluation and a postural control evaluation on a force platform (Synapsys), with or without visual information (eyes open (EO)/eyes closed (EC)). These two latter conditions performed either without orthoses, or with compression garments (CG), or insoles, or both. Results showed that patients did not exhibit a substantial perceived tilt of the visual vertical in the direction of the body tilt (Aubert effect) as did the control subjects. Interestingly, such differential effects were only apparent when the rod was initially positioned to the left of the vertical axis (opposite the longitudinal body axis). In addition, patients showed greater postural instability (sway area) than the controls. The removal of vision exacerbated this instability, especially in the mediolateral (ML) direction. The wearing of orthoses improved postural stability, especially in the eyes-closed condition, with a particularly marked effect in the anteroposterior (AP) direction. Hence, this study suggests that hEDS is associated with changes in the relative contributions of somatosensory and vestibular inputs to verticality perception. Moreover, postural control impairment was offset, at least partially, by wearing somatosensory orthoses.
Keywords: subjective vertical, proprioception, compressive garments, proprioceptive insoles, postural sway
INTRODUCTION
The Ehlers-Danlos syndrome (EDS) is a heterogeneous group of hereditary connective tissue diseases, which are present in at least 1/5000 individuals with a majority of women (Sobey, 2014). Degradation of the composition and elasticity of connective tissue results in a broad, pronounced and unspecific symptomatology. Consequently, the revised Brighton criteria classified EDS in six subtypes, according to the predominance of their clinical manifestations (Beighton et al., 1998). The EDS hypermobility subtype (hEDS) is the most frequently encountered. Besides common symptoms with other subtypes such as fatigue and pain, hEDS is characterized by generalized joint hypermobility combined with variable cutaneous hyperelasticity and proprioceptive impairment (Beighton et al., 1998; Castori, 2012). Indeed, few studies that have investigated proprioceptive sensitivity (i.e., joint position sense) in hEDS, have demonstrated the existence of proprioceptive impairment in this population (Rombaut et al., 2010a; Clayton et al., 2015). A strong hypothesis to explain the neurophysiological basis of this impairment suggests that the generalized joint hypermobility specific to hEDS induces excessive and repeated extension of the ligaments, which damages the surrounding proprioceptive receptors (Ruffini’s and Pacini’s corpuscles; Golgi tendon organs). Additionally, changes in cutaneous elasticity probably affects pressure information transmitted by cutaneous tactile mechanoreceptors to cortical areas. Hence, it is likely that hEDS induces not only a proprioceptive deficit but, more broadly, a somatosensory deficit. Consequently, the major functional disabilities expressed by these patients, including clumsiness and falls, which sometimes lead to kinesiophobia, could be the result of this somatosensory impairment (Rombaut et al., 2012).
Indeed, somatosensory information, arising from muscles, skin, and joints, plays a key role in perception, balance and, more broadly in movement. Currently, there is growing evidence that balance and movement are both based on heteromodal integration of three types of sensory modality, visual, vestibular, and somatosensory, which carry redundant, specific and complementary information (Massion, 1992; Lacour et al., 1997). The integration of these sensory modalities by the central nervous system provides three spatial frames of reference—egocentric (i.e., body), geocentric (i.e., gravity) and allocentric (i.e., external cues)—which contribute to the development of internal models crucially involved in balance and movement (Gurfinkel et al., 1981; Massion, 1994;
Mergner and Rosemeier, 1998). In the sensorimotor processes, internal models refer to a neural process responsible for synthesizing information from sensory modalities and combine efferent and afferent information to resolve sensory ambiguity (Merfeld et al., 1999). Furthermore, sensory processing is a flexible mechanism (Peterka, 2002). The central nervous system continually modulates weight assigned to each sensory modality to provide a dynamic internal representation, making it possible to always generate an appropriate muscle response to maintain and adapt balance to the continuously changing environment (Van der Kooij et al., 2001; Zupan et al., 2002;
Peterka and Loughlin, 2004; Logan et al., 2014). Within
this process, the somatosensory system specifically provides information about the position of different parts of the body with respect to one another. Moreover, it allows characterization and localization of touch and pain (Dijkerman and De Haan, 2007). Thus, the somatosensory system mainly contributes to the sensorimotor map of body space in internal models, an unconscious process also called the ‘‘body schema’’ (De Vignemont, 2010).
Mittelstaedt (1983) reported that information provided by proprioception contributes considerably to the maintenance of body verticality. The perception of vertical is considered be the outcome of synthesizing visual, somatosensory and vestibular information (Brandt et al., 1994; Bisdorff et al., 1996;
Merfeld et al., 1999; Van Beuzekom and Van Gisbergen, 2000;
Bronstein et al., 2003; Barbieri et al., 2008; Pérennou et al., 2008; Tarnutzer et al., 2009). However, it is known that the contribution of each sensory modality in verticality perception varies between subjects and, to a greater extent, in populations presenting either vestibular impairments (e.g., patients with unilateral vestibular loss; Lopez et al., 2008) or somatosensory impairments (e.g., stroke patients with a hypoesthesia pressure and paraplegic patients; Barra et al., 2010). Interestingly, the Aubert effect, consisting in tilting of the visual vertical towards the body during lateral body tilt due to the resultant of the gravitational vector (i.e., perception of the otolith organ) and the idiotropic vector (i.e., perception of the main longitudinal axis of the body), is modified in favor of gravitational vector proportionally to the degree of somatosensory impairment (Barra et al., 2010). Hence, it seems reasonable to inquire whether somatosensory impairment in hEDS patients might modify the Aubert effect. At the same time, it has been previously shown that hEDS patients develop body schema disorders resulting in partial loss of movement control (Rombaut et al., 2010b) and postural instability (Galli et al., 2011). This deterioration in postural stability is manifested in both static (standing) and dynamic (walking) conditions (Rombaut et al., 2011; Rigoldi et al., 2013). Previous studies have already shown a strong connection between somatosensory impairments and balance disorders, especially in Parkinson’s disease (Jacobs and Horak, 2006; Vaugoyeau et al., 2011). Typically, these patients, as in normal aging, compensate for their sensory deficit by an overreliance on visual information (Lord and Webster, 1990;
Isableu et al., 1997; Azulay et al., 2002). Therefore, one can speculate that somatosensory impairment could be responsible to a large extent for this postural instability, and that it could be compensated for by using a high level of visual information.
Compression garments (CG) have been tested empirically in clinical practice in hEDS, resulting in beneficial effects on pain, fatigue and mobility. Speculatively, the CG, due to their mechanical effect, are thought to enhance joint coaptation and increase the pressure of the subcutaneous connective tissue to a normal range. Hence, CG may enhance somatosensory feedback to the brain and, thus, its contribution to postural control. Similarly, proprioceptive insoles (PI) may enhance plantar cutaneous afferents and postural stability.
Therefore, somatosensory orthoses (i.e., CG and PI) offer a
therapeutic solution to reduce somatosensory impairments, however weakly evaluated. Along with these observations, previous studies have demonstrated that CG induced an improvement in knee proprioception, and PI decreased the attentional demand for gait (Clark et al., 2014; Ghai et al., 2016). Conversely, these two ortheses showed no impact in healthy young subjects, and CG appeared to induce a deterioration of postural stability in elderly subjects (Hijmans et al., 2009; Dankerl et al., 2016). In the light of these conflicting observations, we aimed to quantify the impact of these somatosensory orthoses on postural stability in a population with a specific impairment of the somatosensory system. Indeed, it seems plausible that, although the wearing of CG has probably no immediate impact on the damaged joint proprioceptive receptors, its compressive effect applied to subcutaneous connective tissue could allow better somatosensory transmission from cutaneous tactile mechanoreceptors. Hence, somatosensory deficit could be partially reduced by CG, which would compensate for joint proprioception impairment.
Similarly, enhanced plantar cutaneous afferents induced by PI could increase the available sensory information for postural control.
The goal of the present study was to assess: (i) the impact of somatosensory deficit on subjective visual vertical (SVV) and postural stability; and (ii) the effects of somatosensory orthoses (i.e., CG and PI) on static postural control. We hypothesized that: (i) somatosensory impairments would modify SVV, strongly impair postural stability and increase the use of visual information; and (ii) enhancing somatosensory feedback with the orthoses would restore the balance in the use of sensory modalities, thus reducing the use of visual information, and consequently enhance postural stability.
MATERIALS AND METHODS Study Population
Six patients with hEDS (6 females; mean age ± SD:
37 ± 10.41 years) and six healthy, age- and gender-matched control subjects (6 females; mean age ± SD: 36 ± 11.52 years) participated in this study. Patient selection was carried out in the Internal Medicine Department of Caen University Hospital.
Inclusion criteria were based on the revised Villefranche criteria, including the presence of generalized joint hypermobility, skin hyperelasticity, chronic musculoskeletal pain, and/or a positive family history (Beighton et al., 1998). Additionally, patients must have reported hypersensoriality (e.g., a low hearing threshold). Exclusion criteria were: (i) wearing of somatosensory orthoses (i.e., PI and CG); (ii) inability to maintain a minimum of postural stability in static conditions (i.e., holding an upright stance during 1 min); (iii) treatment by a physical therapist; and (iv) other pathologies that directly impact postural control (e.g., Ménière’s disease). Finally, patients were checked for vestibular disorders by ENT examination with otolithic myogenic evoked potentials, and videonystagmography.
Healthy controls subjects were recruited by local phone call.
Control subjects were excluded if they had a neurologic (with
a special focus on vestibular disease using the Fukuda test;
Fukuda, 1959) or orthopedic disorder (analysis of foot plantar pressure distributions using a podoscope) that could affect their postural stability, and a generalized disease affecting joints, or a Beighton score >4/9.
All subjects were treated in strict compliance with the Declaration of Helsinki. The protocol was approved by the CERSTAPS (Ethical Committee of Sport and Physical Activities Research), Notice Number: 2016-26-04-13, approved by the National Academic Commission (CNU) on April 26, 2016.
Written informed consent was obtained from all participants.
Instrumentation
Somatosensory Orthoses
The CG and PI required in this study were customized based on the needs of each patient by orthotic and prosthetic practitioners (Novatex Medical). CG included pants, vest, and mittens, which covered the entire body of all participants (i.e., trunk, upper and lower limbs; Figure 1).
Postural Control
Postural sway was recorded using a motorized force platform (SYNAPSYS, France). Three strain gauges integrated into the force platform recorded the vertical ground reaction force component. The data were sampled at 100 Hz and transformed by computer-automated stability analysis software (i.e., Synapsys software) to obtain x-y coordinates of the center of pressure (COP).
Subjective Visual Vertical
Perception of the vertical was assessed by the SVV test using the Perspective System r (Framiral r , France).
FIGURE 1 | (A) Compression garments (CG) and (B) proprioceptive insoles
(PI) worn by an Ehlers-Danlos syndrome hypermobility type (hEDS) patient
during the experiment.
Experimental Procedure
In the first part of the experiment, participants underwent postural control assessment (duration: 1 h 45 min for patients, and 20 min for controls) followed by SVV assessment (duration:
15 min for all participants).
Subjective Visual Vertical Assessment
To assess the SVV, each participant, in a completely darkened room, was shown, in front of them, the projection of a luminous rod (laser line 2 m in length placed 3 m in front of them).
Participants could rotate the rod around its center in the clockwise or counterclockwise directions using a transmitter, and were instructed to place the rod vertically with respect to the true gravitational vertical. All subjects performed the SVV test in three conditions: standing, sitting and lying on their right side. In this latter condition, participants lay in a standard position on a stretcher with an adjustable head-rest, which was positioned identically initially for each participant (body and head were tilted, respectively, at 90 ◦ and 72 ◦ ). Subjects were asked to minimize their movements during the tests.
Each condition comprised four trials: two with the rod initially oriented to the right side (i.e., 30 ◦ to the right—clockwise) and two to the left side (i.e., − 30 ◦ to the left—counterclockwise).
The tests and conditions were randomly distributed within each participant.
Postural Control Assessment
Postural sway was measured for 52 s while participants stood on a force platform. Participants were asked to stand still, barefoot, arms hanging freely, feet positioned at an angle of 30 ◦ , and to focus on a visual reference mark fixed 1.5 m in front of them in their individual line of vision. The assessment comprised four conditions with two tests each lasting 52 s, with a 20 s rest between each test, and 5 min between each condition. The start and stop signals were given 3 s before and 3 s after each acquisition. The four conditions were: (1) control condition (CC;
without orthoses); (2) CG; (3) PI; and (4) the combination of CG and PI (CG-PI). Each condition was performed with either eyes open (EO) or eyes closed (EC). Participants also underwent dual-task (combining postural control with a cognitive task) and dynamic (sinusoidal translation of support) trials under the four above-mentioned conditions (results are not included in the present article). To minimize any order effects during testing, such as fatigue effects, all conditions and trials (EO/EC) were randomized among subjects. A training test was performed before testing (Figure 2).
Data Analysis
Subjective Visual Vertical Analysis
SVV evaluation error was scored in degrees of deviation from the vertical. Mean errors were calculated across conditions, according to the initial orientation of the rod. Errors were scored negatively when the subjective vertical was oriented to the left, and positively when it was oriented to the right.
Postural Control Analysis
Postural sway parameters calculated from the COP recordings were as follows: the anteroposterior and mediolateral sway standard deviation (SD-AP/SD-ML; mm) and the sway area (AREA-CE; mm 2 ) corresponding to the 95% confidence elliptic area included within the COP path.
Statistical Analysis
The SVV (angle of deviation from the vertical) and postural (AREA-CE, SD-AP and SD-ML) dependent variables failed to display an acceptable normal distribution (Shapiro-Wilk test).
Consequently, non-parametric tests were used for statistical analysis.
The Mann-Whitney U-test was used to compare healthy controls to hEDS patients on verticality perception and postural stability. A Friedman test was used to determine differences between the performances carried out in each postural condition (CC, CG, PI and CG/PI) and each SVV condition (standing, seated, lying: right and left initial orientation). When the result of the Friedman test was significant, we subsequently used a Wilcoxon test for matched samples to determine the effects of vision (EO and EC) and somatosensory orthoses on postural stability. We used the Bonferroni method to correct for multiple comparisons.
Statistical significance was set at 0.05. Statistica (version 10, Statsoft, Inc., Tulsa, OK, USA) was used to perform all analyses.
RESULTS
Subjective Visual Vertical
We first analyzed perception of the visual vertical in each position (standing, seated, lying on the right side) using the Mann-Whitney U-test. In standing condition, hEDS patients oriented the vertical more in left side than controls, when the initial orientation of the rod was also on the left (U = 4, p = 0.026).
Simultaneously, in lying on the right condition, when the initial orientation of the rod was on the left, patients did not exhibit the substantial perceived tilt of the visual vertical in the direction of the body tilt (Aubert effect), and oriented their vertical closer to the real vertical compared to controls, (U = 0, p = 0.002).
Interestingly, in sitting condition, perception of visual vertical was similar in both groups (Figure 3).
The Friedman test revealed significant differences in verticality perception according to the initial orientation of the rod (right and left) and body position (sitting, standing and lying on the right) in hEDS patients (p = 0.0001) and controls (p = 0.00034). As 30 side-by-side comparisons were carried out for each post hoc analysis, the Bonferroni method was used to correct the significance level at 0.0016. Consequently, all the results from the Wilcoxon test reported below with a p > 0.0016 have been used because of our small sample size, and thus have a descriptive vocation.
Regardless of the position, the initial orientation of the rod
seems to influence the verticality perception of hEDS patients
(sitting: Z = 2.20, p = 0.027; standing: Z = 2.20, p = 0.027;
FIGURE 2 | Design of the postural control assessment.
lying: Z = 2.20, p = 0.027). When the initial orientation of the rod was to the right, patients showed a greater degree of deviation of verticality perception in standing compared to sitting (Z = 2.20, p = 0.027), and to a larger extent, when lying compared to sitting (Z = 2.20, p = 0.027) and standing (Z = 2.20, p = 0.027). In contrast, no difference was observed when the initial orientation of the rod was to the left. Likewise, in controls, the initial orientation of the rod did not influence verticality perception. In addition, controls presented a greater deviation of their verticality perception when lying as opposed to sitting and standing, regardless the initial orientation of the rod (right initial orientation: sitting vs. lying: Z = 2.20, p = 0.027, standing vs. lying: Z = 2.20, p = 0.027; left initial orientation:
sitting vs. lying: Z = 2.20, p = 0.027, standing vs. lying: Z = 2.20, p = 0.027).
Postural Control without Somatosensory Orthoses
Compared with controls, hEDS patients showed impaired postural stability, as reflected by their increased sway area (EO, U = 4, p = 0.052) and increased AP sway SD (EO, U = 3,
p = 0.015). These latter effects became more pronounced in the absence of visual information (AREA-CE: EC, U = 2, p = 0.017;
SD-AP: EC, U = 0, p = 0.004). Furthermore, postural stability also deteriorated in the ML direction without vision (U = 4, p = 0.052). Besides, the Wilcoxon test comparing EO and EC revealed an increased sway area (Z = 2.022, p = 0.043) and an increased ML sway SD in hEDS patients (Z = 2.022, p = 0.043).
Removal of vision had no effect on postural stability in controls (Figure 4).
Postural Control with Somatosensory Orthoses
The Friedman test was conducted to assess the effects of
somatosensory orthoses on postural stability in hEDS patients
in four conditions (control, PI, CG, and PI-CG), with (EO)
and without (EC) vision. Then, as six side-by-side comparisons
were carried out within each post hoc analysis, the significance
threshold was set at 0.00833, as indicated by Bonferroni
correction. Similar to the SSV, all the results from the Wilcoxon
test reported below with a p > 0.00833 have a descriptive
vocation.
FIGURE 3 | Comparison of subjective visual vertical (SVV) performance between hEDS patients and controls in different body positions: (A) standing, (B) sitting and (C) lying on the right side. SVV was measured by presenting a laser rod 12 times in total darkness with a 30-degree deviation from the vertical alternately on the right and the left. Subjects were asked to reposition the rod vertically using a remote control. Box plots represent median and quartiles, and dots represent performance of each participant as follows: controls: black; patient 1: red; patient 2: green; patient 3: purple; patient 4: light blue; patient 5: orange; patient 6: dark blue.
∗p < 0.05,
∗∗∗